Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Mapping multiple features in the population response of visual cortex

Nature volume 423, pages 986–990 (2003)Cite this article

Abstract

Stimulus features such as edge orientation, motion direction and spatial frequency are thought to be encoded in the primary visual cortex by overlapping feature maps arranged so that the location of neurons activated by a particular combination of stimulus features can be predicted from the intersections of these maps1,2,3,4,5,6,7,8. This view is based on the use of grating stimuli, which limit the range of stimulus combinations that can be examined. We used optical imaging of intrinsic signals9 in ferrets to assess patterns of population activity evoked by the motion of a texture (a field of iso-oriented bars). Here we show that the same neural population can be activated by multiple combinations of orientation, length, motion axis and speed. Rather than reflecting the intersection of multiple maps, our results indicate that population activity in primary visual cortex is better described as a single map of spatiotemporal energy.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Systematic shifts in the population response induced by changes in axis of motion.
Figure 2: Systematic shifts in the population response induced by changes in bar length.
Figure 3: Shifts in the population response induced by changes in stimulus speed.
Figure 4: Tuning shifts seen with imaging occur at the single unit level.

References

  1. Hubel, D. H. & Wiesel, T. N. Ferrier Lecture: Functional architecture of macaque monkey visual cortex. Proc. R. Soc. Lond. B 198, 1–59 (1977)

    Article  ADS  CAS  Google Scholar 

  2. Hubener, M., Shoham, D., Grinvald, A. & Bonhoeffer, T. Spatial relationships among three columnar systems in cat area 17. J. Neurosci. 17, 9270–9284 (1997)

    Article  CAS  Google Scholar 

  3. Swindale, N. V. How many maps are there in visual cortex? Cereb. Cortex 10, 633–643 (2000)

    Article  CAS  Google Scholar 

  4. Swindale, N. V., Shoham, D., Grinvald, A., Bonhoeffer, T. & Hubener, M. Visual cortex maps are optimized for uniform coverage. Nature Neurosci. 3, 822–826 (2000)

    Article  CAS  Google Scholar 

  5. Issa, N. P., Trepel, C. & Stryker, M. P. Spatial frequency maps in cat visual cortex. J. Neurosci. 20, 8504–8514 (2000)

    Article  CAS  Google Scholar 

  6. Everson, R. M., Prashanth, A. K., Gabbay, M., Knight, B. W., Sirovich, L. & Kaplan, E. Representation of spatial frequency and orientation in the visual cortex. Proc. Natl Acad. Sci. USA 95, 8334–8338 (1998)

    Article  ADS  CAS  Google Scholar 

  7. Shmuel, A. & Grinvald, A. Functional organization for direction of motion and its relationship to orientation maps in cat area 18. J. Neurosci. 16, 6945–6964 (1996)

    Article  CAS  Google Scholar 

  8. Weliky, M., Bosking, W. H. & Fitzpatrick, D. A systematic map of direction preference in primary visual cortex. Nature 379, 725–728 (1996)

    Article  ADS  CAS  Google Scholar 

  9. Bonhoeffer, T. & Grinvald, A. in Brain Mapping: The Methods (eds Toga, A. W. & Mazziotta, J. C.) 55–97 (Academic, New York, 1996)

    Google Scholar 

  10. Wuerger, S., Shapley, R. & Rubin, N. ‘On the visually perceived direction of motion’ by Hans Wallach, 60 years later. Perception 25, 1317–1367 (1996)

    Article  Google Scholar 

  11. Adelson, E. H. & Movshon, J. A. Phenomenal coherence of moving visual patterns. Nature 300, 523–525 (1982)

    Article  ADS  CAS  Google Scholar 

  12. De Valois, R. L. & De Valois, K. K. Spatial Vision (Oxford Univ. Press, New York, 1988)

    MATH  Google Scholar 

  13. Lorenceau, J., Shiffrar, M., Wells, N. & Castet, E. Different motion sensitive units are involved in recovering the direction of moving lines. Vision Res. 33, 1207–1217 (1993)

    Article  CAS  Google Scholar 

  14. Pack, C. C. & Born, R. T. Temporal dynamics of a neural solution to the aperture problem in visual area MT of macaque brain. Nature 409, 1040–1042 (2001)

    Article  ADS  CAS  Google Scholar 

  15. Shoham, D., Hubener, M., Schulze, S., Grinvald, A. & Bonhoeffer, T. Spatio-temporal frequency domains and their relation to cytochrome oxidase staining in cat visual cortex. Nature 385, 529–533 (1997)

    Article  ADS  CAS  Google Scholar 

  16. Hubel, D. H. & Wiesel, T. N. Receptive fields and functional architecture in two non-striate visual areas (18 and 19) of the cat. J. Neurophysiol. 28, 229–289 (1965)

    Article  CAS  Google Scholar 

  17. Gilbert, C. D. Laminar differences in receptive field properties of cells in cat primary visual cortex. J. Physiol. (Lond.) 268, 391–421 (1977)

    Article  CAS  Google Scholar 

  18. Skottun, B. C., Zhang, J. & Grosof, D. H. On the direction selectivity of cells in the visual cortex to drifting dot patterns. Vis. Neurosci. 11, 885–897 (1994)

    Article  CAS  Google Scholar 

  19. Movshon, J. A., Thompson, I. D. & Tolhurst, D. J. Spatial summation in the receptive fields of simple cells in the cat's striate cortex. J. Physiol. (Lond) 283, 53–77 (1978)

    Article  CAS  Google Scholar 

  20. Movshon, J. A., Thompson, I. D. & Tolhurst, D. J. Receptive field organization of complex cells in the cat's striate cortex. J. Physiol. (Lond.) 283, 79–99 (1978)

    Article  CAS  Google Scholar 

  21. De Valois, K. K., De Valois, R. L. & Yund, E. W. Responses of striate cortex cells to grating and checkerboard patterns. J. Physiol. (Lond.) 291, 483–505 (1979)

    Article  CAS  Google Scholar 

  22. Gizzi, M. S., Katz, E., Schumer, R. A. & Movshon, J. A. Selectivity for orientation and direction of motion of single neurons in cat striate and extrastriate visual cortex. J. Neurophysiol. 63, 1529–1543 (1990)

    Article  CAS  Google Scholar 

  23. Hammond, P. & Smith, A. T. Directional tuning interactions between moving oriented and textured stimuli in complex cells of feline striate cortex. J. Physiol. (Lond.) 342, 35–49 (1983)

    Article  CAS  Google Scholar 

  24. Skottun, B. C., Grosof, G. H. & De Valois, R. L. Responses of simple and complex cells to random dot patterns: a quantitative comparison. J. Neurophysiol. 59, 1719–1735 (1988)

    Article  CAS  Google Scholar 

  25. Geisler, W. S., Albrecht, D. G., Crane, A. M. & Stern, L. Motion direction signals in the primary visual cortex of cat and monkey. Vis. Neurosci. 18, 501–516 (2001)

    Article  CAS  Google Scholar 

  26. Galuske, R. A. W., Schmidt, K. E., Kluge, T. & Singer, W. Motion and velocity representation in cat primary visual cortex. Soc. Neurosci. Abstr. vol. 27. Program No. 164.2 (2001)

  27. Carandini, M., Heeger, D. J. & Movshon, J. A. in Cerebral Cortex (ed. Ulinski, P. S.) vol. 13, 401–443 (Kluwer Academic/Plenum, New York, 1999)

    Book  Google Scholar 

  28. Adelson, E. H. & Bergen, J. R. Spatiotemporal energy models for the perception of motion. J. Opt. Soc. Am. A 2, 284–299 (1985)

    Article  ADS  CAS  Google Scholar 

  29. White, L. E., Bosking, W. H., Williams, S. M. & Fitzpatrick, D. Maps of central visual space in ferret V1 and V2 lack matching inputs from the two eyes. J. Neurosci. 19, 7089–7099 (1999)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank D. Purves, J. A. Movshon, S. Nundy, J. C. Crowley and members of the Fitzpatrick laboratory for helpful discussions. This work was supported by a grant from the National Institutes of Health to D.F.

Author information

Authors and Affiliations

  1. Department of Neurobiology and Department of Community and Family Medicine, Duke University Medical Center, Durham, North Carolina, 27710, USA

    Amit Basole, Leonard E. White & David Fitzpatrick

Authors
  1. Amit Basole
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leonard E. White
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David Fitzpatrick
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David Fitzpatrick.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Basole, A., White, L. & Fitzpatrick, D. Mapping multiple features in the population response of visual cortex. Nature 423, 986–990 (2003). https://doi.org/10.1038/nature01721

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01721

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing